Control of visuo-spatial attention. Emiliano Macaluso

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1 Control of visuo-spatial attention Emiliano Macaluso

2 CB demo

3 Attention Limited processing resources Overwhelming sensory input cannot be fully processed => SELECTIVE PROCESSING

4 Selection via spatial orienting time Shifts of gaze and/or covert attention to select relevant locations Sequential processing of relevant information for in-depth analysis

5 OVERVIEW BEHAVUIOURAL PARADIGMS Visual search Spatial cueing NEURAL SUBSTRATES Hemi-spatial Neglect Electrophysiology (non-human primates) ATTENTION NEWORKS IN HUMANS Dorsal and ventral attention networks Source-Site model of attention control Interactions between networks nodes

6 Behavioral paradigms: visual search CONJUNCTION SERACH POP-OUT (FEATURE) SERACH o x o x o x o o o o x x x o o Search for the red X x o o x x o o o x o x o o x o Result: => Pop-out search is fast and does not depend on the number of distractors (stimulus-driven orienting) => Conjunction of features requires topdown attention to the items

7 Behavioral paradigms: spatial cueing (Posner 80) ENDOGENOUS ATTENTION: based on voluntary decisions (e.g. strategy, goals, knowledge) EXOGENOUS ATTENTION: based on incoming signal (e.g. sudden onsets, high contrast) Top-down control by internal signals Bottom-up control by external signals Standard spatial cueing paradigms > cue + + x target + x

8 Behavioral paradigms: spatial cueing (Posner 80) Valid trial Fixation time X CUE TARGET

9 Behavioral paradigms: spatial cueing (Posner 80) Valid trial Invalid trial Fixation time X CUE TARGET X

10 Behavioral paradigms: spatial cueing (Posner 80) Valid trial Invalid trial Fixation CUE time X TARGET X Result: Covert discrimination is faster and more accurate for valid trials than invalid trials Interpretation: - Benefits of endogenous attention at the attended side (valid trials) - Costs of stimulus-driven shift of attention from cued to target location (invalid trials)

11 Neural substrates: hemi-spatial neglect Failure to orient (attend) towards the contralesional side of space Typically following lesion of the right ventral fronto-parietal network

12 Neural substrates: hemi-spatial neglect Visual search Spatial cueing Search for T target among L-distractors Leftward bias in overt spatial orienting Selective deficit for left invalid trials (i.e. cue right, target left) => disengagement deficit

13 Neural substrates: electrophysiology (non-human) The main players: LIP (lateral intraparietal sulcus) FEF (frontal eye-feields) Frontal node Visual areas: V1-V2-V4 MT Parietal node

14 Neural substrates: electrophysiology (non-human) Activity in parietal cortex (LIP) reflects attention, rather than movement preparation Small sensory response: stimulus irrelevant / unattended Large response, before the eye-movement: stimulus is relevant/attended! Large response, with arm rather than eye-movement: stimulus still relevant/attended Eg. Colby and Goldberg 1999

15 Neural substrates: electrophysiology (non-human) Attention modulates sensory responses in the visual cortex Neuron in area V2 Neuron in area V4 Review Treue 2001 Moran and Desimone, 1985 Note: visual input does not change, what changes is the focus of covert attention

16 preferred orientation Neural substrates: electrophysiology (non-human) Competition (bottom-up) between two stimuli in the neuron s RF reduces the response to the preferred stimulus Top-down attention modulate these competitive interactions, e.g. => Based competition model of attention (Desimone 1998)

17 Tasks and substrates: summary Visual search and spatial cueing Attention selects relevant information Multiple types of signals: endogenous (voluntary) & exogenous (stimulus-driven) Neural Substrates Neglect: leftward bias after lesion of the right fronto-parietal cortex Attention modulates activity in: fronto-parietal cortex (FEF and LIP) & visual occipital cortex

18 OVERVIEW BEHAVUIOURAL PARADIGMS Visual search Spatial cueing NEURAL SUBSTRATES Hemi-spatial Neglect Electrophysiology (non-human primates) ATTENTION NEWORKS IN HUMANS Dorsal and ventral attention networks Source-Site model of attention control Interactions between networks nodes

19 Selection via spatial orienting time Shifts of gaze and/or covert attention to select relevant locations Sequential processing of relevant information for in-depth analysis

20 Attention network for attention shifting => predictable shifts of attention: voluntary/endogenous control? Frontal cortex (FEF) FEF IPS Parietal cortex (IPS) => The dorsal fronto-parietal network Corbetta et al. 1993

21 Attention shifting: endogenous vs. exogenous control Search: goal-driven (endogenous) orienting Eye-position (n. fixations) + Serial processing during search Target :

22 Attention shifting: endogenous vs. exogenous control Search: goal-driven (endogenous) orienting Eye-position (n. fixations) + Serial processing during search Target : Track: stimulus-driven (exogenous) orienting Eye-position (n. fixations) +

23 Attention shifting: endogenous vs. exogenous control Search: goal-driven (endogenous) orienting IPS/PPC FEF => The dorsal fronto-parietal network Vis Track: stimulus-driven (exogenous) orienting TPJ => The ventral fronto-parietal network (posterior node only, here)

24 Attention shifting: spatial cueing Result: Covert discrimination is faster and more accurate for valid trials than invalid trials Interpretation: - Benefits of endogenous attention at the attended side (valid trials) - Costs of stimulus-driven shift of attention from cued to target location (invalid trials)

25 fmri using spatial cueing paradigms Central detection Blocked design: valid & invalid vs. central attention Parietal cortex (P) Frontal eye-field (F) Superior temporal sulcus (ST) Temporo-occipital junction (TO) Precuneus (PCU) => The dorsal fronto-parietal network, but endo/exo mixed-up Gitelman et al. 1999

26 Task analysis Multiple processes occur during this type of task Left Right CUE-related voluntary (endogenous) processes (voluntary shift + sustained delay)

27 Task analysis Multiple processes occur during this type of task Left Time Left Right Right Valid trial: Facilitation sensory processing CUE-related voluntary (endogenous) processes (voluntary shift + sustained delay)

28 Task analysis Multiple processes occur during this type of task Left Time Left Right Right Valid trial: Facilitation sensory processing CUE-related voluntary (endogenous) processes (voluntary shift + sustained delay) Left Right Time Invalid trial: Spatial re-orienting ( stimulus-driven )

29 fmri of spatial re-orienting Event-related fmri: direct comparison invalid > valid trials Valid trial Invalid trial > + x x > + cue-related (endogenous) effects will cancel out Arrington et al. (2002) Corbetta and Shulman (2002) Macaluso et al. (2002) TPJ: temporo-parietal junction & IFG: inferior frontal gyurs => The ventral fronto-parietal network (exogenous control)

30 Facilitation at the attended side Pioneering PET study of endogenous spatial attention (Heinze at al.,1994) Stimuli on both sides, sustained (blocked) attention to one side => Modulation of contralateral visual activity during endogenous control

31 % signal change Cue-related, preparatory activity Participants are CUED to one location, prior to the onset of the target stimulus Dorsal fronto-parietal network Preparatory Attention Attention + Stimulation Cue Stimulation Time => Preparatory shifts of baseline activity, in dorsal FP-network Kastner et al. 1999

32 % signal change % signal change Cue-related, preparatory activity Dorsal fronto-parietal network Preparatory Attention Attention + Stimulation Cue Stimulation Time Sensory visual cortex V 4 Time (sec) => Preparatory shifts also in VISUAL occipital cortex => Possible role of back-projections Kastner et al. 1999

33 Visuo-spatial attention control: interim summary Multiple processes for attentional control Endogenous orienting (cue) : Dorsal fronto-parietal Network Exogenous re-orienting (invalid trials) : Ventral fronto-parietal Network Sensory facilitation (valid trials) : Occipital Cortex Cue-related preparatory activity: Dorsal FP-net + occipital cortex Dorsal FP-net Ventral FP-net Visual, sensory

34 Visuo-spatial attention control: interim summary Left Right Invalid trial Spatial re-orienting => Ventral FP-net Macaluso et al., 2002; Macaluso et al., 2003

35 Visuo-spatial attention control: interim summary Valid trial Left Right Modulation of sensory input => sensory areas Invalid trial Spatial re-orienting => Ventral FP-net Macaluso et al., 2002; Macaluso et al., 2003

36 Visuo-spatial attention control: interim summary Valid trial Left Right Preparatory activity Modulation of sensory input => sensory areas Invalid trial => Dorsal FP-net Spatial re-orienting => Ventral FP-net Macaluso et al., 2002; Macaluso et al., 2003

37 Visuo-spatial attention control: interim summary BUT ALSO : Left Right Preparatory activity Attend: Target: -2 L R L R Present ABSENT Preparatory Effects in Sensory Areas => Dorsal FP-net Macaluso et al., 2002; Macaluso et al., 2003

38 SITE SOURCE Source-Site model of attention control Dorsal Fronto-Parietal Network (PPC, FEF) Ventral Fronto-Parietal Network (TPJ, IFG) Sensory Areas (Occipital Cortex) Modified from Corbetta & Schulman, 2002; see also Kastner et al., 1999; plus Macaluso & Driver, 2000

39 SITE SOURCE Source-Site model of attention control Top-down Control (endogenous) Dorsal Fronto-Parietal Network (PPC, FEF) Ventral Fronto-Parietal Network (TPJ, IFG) Preparation Expectation Intention Sensory Areas (Occipital Cortex) External world Modified from Corbetta & Schulman, 2002; see also Kastner et al., 1999; plus Macaluso & Driver, 2000

40 SITE SOURCE Source-Site model of attention control Top-down Control (endogenous) Dorsal Fronto-Parietal Network (PPC, FEF) Bottom-up Control (exogenous) Ventral Fronto-Parietal Network (TPJ, IFG) Preparation Expectation Intention Sensory Areas (Occipital Cortex) Salience Relevance External world Modified from Corbetta & Schulman, 2002; see also Kastner et al., 1999; plus Macaluso & Driver, 2000

41 Control of visuo-spatial attention Attention is a dynamic mechanism, NOT the function of a single brain area!!! Any direct evidence for dynamic changes within the Source-Site Network? ==> Use fmri to study task-dependent changes of functional connectivity between brain areas

42 y: right M1 Inter-regional connectivity Correlation between "BOLD in area A and BOLD in area B Example (at Rest): - Seed in left M1 => reveals right M1 2 Predictor / seed : BOLD in the left M Correlation / connectivity Data: "here BOLD in right M1" scans X: left M1

43 Changes of inter-regional connectivity Spatial cueing paradigm Cue: Left / Right Target: Left / Right Invalid - Valid Inferior Parietal Cortex Target Right - Left Left Occipital Cortex Indovina & Macaluso, 2004

44 Changes of inter-regional connectivity Spatial cueing paradigm Cue: Left / Right Target: Left / Right Inferior Parietal Cortex Invalid trials Valid trials Invalid - Valid Inferior Parietal Cortex Occipital Cortex Occipital Signal Target Right - Left Increased connectivity between occipital areas and inferior parietal cortex during invalid trials Left Occipital Cortex

45 Bilinear state equation state changes intrinsic connectivity m external inputs system state direct inputs Cu z B u A z m j j j ) ( 1 m nm n m n m j j nn j n j n j j nn n n n u u c c c c z z b b b b u a a a a z z modulation of connectivity state changes intrinsic connectivity m external inputs system state direct inputs Cu z B u A z m j j j ) ( 1 m nm n m n m j j nn j n j n j j nn n n n u u c c c c z z b b b b u a a a a z z modulation of connectivity Z 1 Z 2 a 12 a 21 b 2 21 u 1 u 2 c 11 "stimuli" "context" The influence one system exerts over another (Friston et al., 1993) => directional / causal effects A-priori specification of stimuli / task (design) and network s areas Effective connectivity

46 Causal influences, during attention control Spatial cueing task with valid and invalid trials judge orientation of the patch circled in green Vossel et al. 2012

47 Causal influences: top-down effects on visual cortex Top-down modulation from IPS (dorsal FP-net) to VIS cortex boosts contralateral & suppresses ipsilateral

48 Causal influences: bottom-up effects for invalid trials Bottom-up activation from VIS to TPJ (ventral FP-net) by invalid targets exogenous signals that further propagate to dorsal regions

49 Control of visuo-spatial attention Attention is a dynamic mechanism, NOT the function of a single brain area!!! Additional evidence for interactions between the nodes of the attention networks: A. Effect of frontal stimulation on visual activity in occipital cortex B. Functional connectivity between dfp and vfp in Neglect

50 Interactions between FEF and VIS: electrophysiology The main players: LIP (lateral intraparietal sulcus) FEF (frontal eye-feields) Visual areas: V1-V2-V4 MT

51 Interactions between FEF and VIS: electrophysiology Micro-stimulation of FEF => record visual responses in V4 Visual activity in V4 Motor effect after suprathresholds FEF stimulation Moore and Armstrong, 2003

52 Interactions between FEF and VIS: electrophysiology Enhanced visual responses in V4, with sub-threshold FEF stimulation (no eye-movement) = preferred stimulus in the neuron s RF FEF as a source of the modulatory (top-down) influences on visual cortex Moore and Armstrong, 2003

53 Interactions between FEF and VIS: TMS in humans TMS on FEF, while recording visual responses with fmri

54 Interactions between FEF and VIS: TMS in humans FEF stimulation enhances visual responses (only at peripheral locations) FEF as a source of (top-down) influences on visual cortex!

55 Interactions between dfp and vfp: Neglect Typically following lesion of the right ventral fronto-parietal network => Dorsal network relatively spared, but

56 Interactions between dfp and vfp: Neglect Lesion anatomy (n = 11; purple, damaged in one to three patients; blue, damaged in four to seven patients) dorsal FP, green ventral FP, red Test pair-wise connectivity (correlation) within- and betweenattention control networks + link behavioral deficits in spatial cuing task He et al., 2007

57 Interactions between dfp and vfp: Neglect Reduced connectivity within the dorsal FP: L-R pips which correlates with the behavioral reorienting deficit! => Dysfunction of the intact dorsal (endogenous) system He et al., 2007

58 Interactions between dfp and vfp: Neglect Reduced connectivity within the ventral FP: L-R STS Acute: L VF, Invalid which also correlates with the behavioral reorienting deficit! He et al., 2007

59 Interactions between dfp and vfp: Neglect Links between reduced connectivity in the two systems Possible role of the MFG as a communication hub between the dorsal and the ventral attention systems He et al., 2007

60 An updated model of dfp-vfp control Corbetta and Shulman 2002 Corbetta et al., 2008 BUT see also (e.g.) Vossel et al, 2012.

61 Summary Multiple processes for attentional control Endogenous orienting (cue) : Dorsal fronto-parietal Network Exogenous re-orienting (invalid trials) : Ventral fronto-parietal Network Sensory facilitation (valid trials): Occipital Cortex Cue-related preparatory activity: Dorsal FP-net + occipital cortex Source-Site Model Endogenous control: Top-down signals (dorsal network) Exogenous control: Bottom-up signals (ventral network) Dynamic changes of connectivity between areas ( source ) and sensory areas ( site ) Dynamic interactions within/between dorsal and ventral source regions

62 CONCLUSIONS Attention selects relevant information Endogenous & exogenous signals Primary role of the fronto-parietal cortex (dfp & vfp) Source-site model of attention control Interactions between the nodes of the attention system Attention is a dynamic mechanism, NOT the function of a single brain area!!!

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